Nitric oxide's reactions with hemoglobin: a view through the SNO-storm (original) (raw)

• Les prix Nobel: 1998. 210–307 (Nobel Foundation, Stockholm, Sweden, 1999).
• Jia, L., Bonaventura, C., Bonaventura, J. & Stamler, J.S. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380, 221–226 (1996).
  Article CAS Google Scholar
• Gow, A.J., Luchsinger, B.P., Pawloski, J.R., Singel, D.J. & Stamler, J.S. The oxyhemoglobin reaction of nitric oxide. Proc. Natl. Acad. Sci. USA 96, 9027–9032 (1999).
  Article CAS Google Scholar
• Stamler, J.S. et al. Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 276, 2034–2037 (1997).
  Article CAS Google Scholar
• Gow, A.J. & Stamler, J.S. Reactions between nitric oxide and haemoglobin under physiological conditions. Nature 391, 169–173 (1998).
  Article CAS Google Scholar
• McMahon, T.J. et al. Nitric oxide in the human respiratory cycle. Nat. Med. 3, 711–717 (2002).
  Article Google Scholar
• Garel, M.C. et al. Covalent binding of glutathione to hemoglobin. I. Inhibition of hemoglobin S polymerization. J. Biol. Chem. 261, 14704–14709 (1986).
  CAS PubMed Google Scholar
• Perutz, M.F. Blood. Taking the pressure off. Nature 380, 205–206 (1996).
  Article CAS Google Scholar
• Doyle, M.P. & Hoekstra, J.W. Oxidation of nitrogen oxides by bound dioxygen in hemoproteins. J. Inorg. Biochem. 14, 351–358 (1981).
  Article CAS Google Scholar
• Herold, S., Exner, M. & Nauser, T. Kinetic and mechanistic studies of the NO*-mediated oxidation of oxymyoglobin and oxyhemoglobin. Biochemistry 40, 3385–3395 (2001).
  Article CAS Google Scholar
• Dou, Y., Maillett, D.H., Eich, R.F. & Olson, J.S. Myoglobin as a model system for designing heme protein based blood substitutes. Biophys. Chem. 98, 127–148 (2002).
  Article CAS Google Scholar
• Gross, S.S. & Lane, P. Physiological reactions of nitric oxide and hemoglobin: a radical rethink. Proc. Natl. Acad. Sci. USA 96, 9967–9969 (1999).
  Article CAS Google Scholar
• Gladwin, M.T. et al. Relative role of heme nitrosylation and β-cysteine 93 nitrosation in the transport and metabolism of nitric oxide by hemoglobin in the human circulation. Proc. Natl. Acad. Sci. USA 97, 9943–9948 (2000).
  Article CAS Google Scholar
• Huang, Z. et al. Nitric oxide binding to oxygenated hemoglobin under physiological conditions. Biochim. Biophys. Acta 1568, 252–260 (2001).
  Article CAS Google Scholar
• Huang, Z. et al. Kinetics of nitric oxide binding to R-state hemoglobin. Biochem. Biophys. Res. Commun. 292, 812–818 (2002).
  Article CAS Google Scholar
• Han, T.H., Hyduke, D.R., Vaughn, M.W., Fukuto, J.M. & Liao, J.C. Nitric oxide reaction with red blood cells and hemoglobin under heterogeneous conditions. Proc. Natl. Acad. Sci. USA 99, 7763–7768 (2002).
  Article CAS Google Scholar
• Zhang, Y. & Hogg, N. Mixing artifacts from the bolus addition of nitric oxide to oxymyoglobin: implications for S-nitrosothiol formation. Free Radic. Biol. Med. 32, 1212–1219 (2002).
  Article CAS Google Scholar
• Joshi, M.S. et al. Nitric oxide is consumed, rather than conserved, by reaction with oxyhemoglobin under physiological conditions. Proc. Natl. Acad. Sci. USA 17, 10341–10346 (2002).
  Article Google Scholar
• Luchsinger, B.P. et al. Routes to S-nitroso-hemoglobin formation with heme redox and preferential reactivity in the β subunits. Proc. Natl. Acad. Sci. USA 100, 461–466 (2003).
  Article CAS Google Scholar
• Fernandez, B.O., Lorkovic, I.M. & Ford, P.C. Nitrite catalyzes reductive nitrosylation of the water-soluble ferri-heme model Fe(III)(TPPS) to Fe(II)(TPPS)(NO). Inorg. Chem. 42, 2–4 (2003).
  Article CAS Google Scholar
• Spencer, N.Y. et al. Reoxygenation/deoxygenation cycles of nitrosylhemoglobin. Free Radic. Biol. Med. 33, S381 (2002).
  Google Scholar
• McMahon, T.J. & Stamler, J.S. Concerted nitric oxide/oxygen delivery by hemoglobin. Meth. Enzymol. 301, 99–114 (1999).
  Article CAS Google Scholar
• Patel, R.P. et al. Biochemical characterization of human S-nitrosohemoglobin. Effects on oxygen binding and transnitrosation. J. Biol. Chem. 274, 15487–15492 (1999).
  Article CAS Google Scholar
• McMahon, T.J., Exton Stone, A., Bonaventura, J., Singel, D.J. & Solomon Stamler, J. Functional coupling of oxygen binding and vasoactivity in S-nitrosohemoglobin. J. Biol. Chem. 275, 16738–16745 (2000).
  Article CAS Google Scholar
• Deem, S., Gladwin, M.T., Berg, J.T., Kerr, M.E. & Swenson, E.R. Effects of S-nitrosation of hemoglobin on hypoxic pulmonary vasoconstriction and nitric oxide flux. Am. J. Respir. Crit. Care Med. 163, 1164–1170 (2001).
  Article CAS Google Scholar
• Deem, S. et al. Effects of S-nitrosation and cross-linking of hemoglobin on hypoxic pulmonary vasoconstriction in isolated rat lungs. Circ. Res. 91, 626–632 (2002).
  Article CAS Google Scholar
• Gladwin, M.T. et al. S-nitrosohemoglobin is unstable in the reductive red cell environment and lacks O2/NO-linked allosteric function. J. Biol. Chem. 21, 27818–27828 (2002).
  Article Google Scholar
• Wolzt, M. et al. Biochemical characterization of S-nitrosohemoglobin. Mechanisms underlying synthesis, no release, and biological activity. J. Biol. Chem. 274, 28983–28990 (1999).
  Article CAS Google Scholar
• Hobbs, A., Gladwin, M., Patel, R., Williams, D. & Butler, A. Haemoglobin: NO transporter, NO inactivator or NOne of the above? Trends Pharmacol. Sci. 23, 406–411 (2002).
  Article CAS Google Scholar
• Agvald, P., Adding, L.C., Artlich, A., Persson, M.G. & Gustafsson, L.E. Mechanisms of nitric oxide generation from nitroglycerin and endogenous sources during hypoxia in vivo. Br. J. Pharmacol. 135, 373–382 (2002).
  Article CAS Google Scholar
• Crawford, J.H., White, R.C. & Patel, R.P. Vasoactivity of S-nitrosohemoglobin: role of oxygen, heme and NO oxidation states. Blood first edition paper, 30 January 2003 (DOI 10.1182/blood-2002-12-3825).
• Marley, R., Feelisch, M., Holt, S. & Moore, K. A chemiluminescense-based assay for S-nitrosoalbumin and other plasma S-nitrosothiols. Free Radic. Res. 32, 1–9 (2000).
  Article CAS Google Scholar
• Jourd'heuil, D., Gray, L. & Grisham, M.B. S-nitrosothiol formation in blood of lipopolysaccharide-treated rats. Biochem. Biophys. Res. Commun. 273, 22–26 (2000).
  Article CAS Google Scholar
• Marley, R. et al. Formation of nanomolar concentrations of S-nitroso-albumin in human plasma by nitric oxide. Free Radic. Biol. Med. 31, 688–696 (2001).
  Article CAS Google Scholar
• Rossi, R. et al. Physiological levels of S-nitrosothiols in human plasma. Circ. Res. 89, E47–E47 (2001).
  Article CAS Google Scholar
• Cannon, R.O. et al. Effects of inhaled nitric oxide on regional blood flow are consistent with intravascular nitric oxide delivery. J. Clin. Invest. 108, 279–287 (2001).
  Article CAS Google Scholar
• Rassaf, T., Bryan, N.S., Kelm, M. & Feelisch, M. Concomitant presence of N-nitroso and S-nitroso proteins in human plasma. Free Radic. Biol. Med. 33, 1590–1596 (2002).
  Article CAS Google Scholar
• Feelisch, M. et al. Concomitant S-, N-, and heme-nitros(yl)ation in biological tissues and fluids: implications for the fate of NO in vivo. FASEB J. 16, 1775–1785 (2002).
  Article CAS Google Scholar
• Rassaf, T. et al. Evidence for in vivo transport of bioactive nitric oxide in human plasma. J. Clin. Invest. 109, 1241–1248 (2002).
  Article CAS Google Scholar
• Rees, D.D., Palmer, R.M., Hodson, H.F. & Moncada, S. A specific inhibitor of nitric oxide formation from L-arginine attenuates endothelium-dependent relaxation. Br. J. Pharmacol. 96, 418–424 (1989).
  Article CAS Google Scholar
• Amezcua, J.L., Palmer, R.M., de Souza, B.M. & Moncada, S. Nitric oxide synthesized from L-arginine regulates vascular tone in the coronary circulation of the rabbit. Br. J. Pharmacol. 97, 1119–1124 (1989).
  Article CAS Google Scholar
• Chu, A. et al. Effects of inhibition of nitric oxide formation on basal vasomotion and endothelium-dependent responses of the coronary arteries in awake dogs. J. Clin. Invest. 87, 1964–1968 (1991).
  Article CAS Google Scholar
• Panza, J.A., Casino, P.R., Kilcoyne, C.M. & Quyyumi, A.A. Role of endothelium-derived nitric oxide in the abnormal endothelium- dependent vascular relaxation of patients with essential hypertension. Circulation 87, 1468–1474 (1993).
  Article CAS Google Scholar
• Quyyumi, A.A. et al. Nitric oxide activity in the human coronary circulation. Impact of risk factors for coronary atherosclerosis. J. Clin. Invest. 95, 1747–1755 (1995).
  Article CAS Google Scholar
• Gladwin, M.T. et al. Role of circulating nitrite and S-nitrosohemoglobin in the regulation of regional blood flow in humans. Proc. Natl. Acad. Sci. USA 97, 11482–11487 (2000).
  Article CAS Google Scholar
• Schechter, A.N., Gladwin, M.T. & Cannon, R.O. NO solutions? J. Clin. Invest. 109, 1149–1151 (2002).
  Article CAS Google Scholar
• Furchgott, R.F. & Zawadzki, J.V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288, 373–376 (1980).
  Article CAS Google Scholar
• Ignarro, L.J., Byrns, R.E., Buga, G.M. & Wood, K.S. Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical. Circ. Res. 61, 866–879 (1987).
  Article CAS Google Scholar
• Ignarro, L.J., Buga, G.M., Wood, K.S., Byrns, R.E. & Chaudhuri, G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. USA 84, 9265–9269 (1987).
  Article CAS Google Scholar
• Palmer, R.M., Ferrige, A.G. & Moncada, S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327, 524–526 (1987).
  Article CAS Google Scholar
• Palmer, R.M., Ashton, D.S. & Moncada, S. Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 333, 664–666 (1988).
  Article CAS Google Scholar
• Coin, J.T. & Olson, J.S. The rate of oxygen uptake by human red blood cells. J. Biol. Chem. 254, 1178–1190 (1979).
  CAS PubMed Google Scholar
• Liu, X. et al. Diffusion-limited reaction of free nitric oxide with erythrocytes. J. Biol. Chem. 273, 18709–18713 (1998).
  Article CAS Google Scholar
• Vaughn, M.W., Kuo, L. & Liao, J.C. Effective diffusion distance of nitric oxide in the microcirculation. Am. J. Physiol. 274, H1705–H1714 (1998).
  CAS PubMed Google Scholar
• Butler, A.R., Megson, I.L. & Wright, P.G. Diffusion of nitric oxide and scavenging by blood in the vasculature. Biochim. Biophys. Acta 1425, 168–176 (1998).
  Article CAS Google Scholar
• Liao, J.C., Hein, T.W., Vaughn, M.W., Huang, K.T. & Kuo, L. Intravascular flow decreases erythrocyte consumption of nitric oxide. Proc. Natl. Acad. Sci. USA 96, 8757–8761 (1999).
  Article CAS Google Scholar
• Vaughn, M.W., Huang, K.T., Kuo, L. & Liao, J.C. Erythrocytes possess an intrinsic barrier to nitric oxide consumption. J. Biol. Chem. 275, 2342–2348 (2000).
  Article CAS Google Scholar
• Huang, K.T. et al. Modulation of nitric oxide bioavailability by erythrocytes. Proc. Natl. Acad. Sci. USA 98, 11771–11776 (2001).
  Article CAS Google Scholar
• Reiter, C.D. et al. Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease. Nat. Med. 8, 1383–1389 (2002).
  Article CAS Google Scholar
• Deem, S., Swenson, E.R., Alberts, M.K., Hedges, R.G. & Bishop, M.J. Red-blood-cell augmentation of hypoxic pulmonary vasoconstriction: hematocrit dependence and the importance of nitric oxide. Am. J. Respir. Crit. Care Med. 157, 1181–1186 (1998).
  Article CAS Google Scholar
• Doherty, D.H. et al. Rate of reaction with nitric oxide determines the hypertensive effect of cell-free hemoglobin. Nat. Biotechnol. 16, 672–676 (1998).
  Article CAS Google Scholar
• Sloan, E.P. et al. Diaspirin cross-linked hemoglobin (DCLHb) in the treatment of severe traumatic hemorrhagic shock: a randomized controlled efficacy trial. JAMA 282, 1857–1864 (1999).
  Article CAS Google Scholar
• Espey, M.G., Thomas, D.D., Miranda, K.M. & Wink, D.A. Focusing of nitric oxide mediated nitrosation and oxidative nitrosylation as a consequence of reaction with superoxide. Proc. Natl. Acad. Sci. USA 99, 11127–11132 (2002).
  Article CAS Google Scholar
• Fox-Robichaud, A. et al. Inhaled NO as a viable antiadhesive therapy for ischemia/reperfusion injury of distal microvascular beds. J. Clin. Invest. 101, 2497–2505 (1998).
  Article CAS Google Scholar
• Stamler, J.S. et al. Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proc. Natl. Acad. Sci. USA 89, 7674–7677 (1992).
  Article CAS Google Scholar
• Lim, D.G. et al. Nitrolinoleate, a nitric oxide-derived mediator of cell function: synthesis, characterization, and vasomotor activity. Proc. Natl. Acad. Sci. USA 99, 15941–15946 (2002).
  Article CAS Google Scholar